systematic and anatomical study of the genus gracilaria in japan

106 Pages·2017·11.08 MB·English

Title SYSTEMATIC AND ANATOMICAL STUDY OF THE GENUS GRACILARIA IN JAPAN
Author(s) YAMAMOTO, Hirotoshi
Citation MEMOIRS OF THE FACULTY OF FISHERIES HOKKAIDO UNIVERSITY, 25(2), 97-152
Issue Date 1978-03
Doc URL http://hdl.handle.net/2115/21865
Type bulletin (article)
File Information 25(2)_P97-152.pdf

Instructions for use
Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP
SYSTEMATIC AND ANATOMICAL STUDY OF THE GENUS
GRACILARIA IN JAPAN*
Hirotoshi YAMAMOTO
Usujiri Fisheries Laboratory, Faculty of Fisheries, Hokkaido University,
Usujiri, Minami-kayabe, Hokkaido, Japan
"
Contents
Page
A_ Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 98
B. Materials and methods .................................................... 100
1. Collecting places ...................................................... 100
2. Methods for microscopic observation .................................... 101
C. General considerations .................................................... 102
1. External form of the frond and basal constriction of the branch ............ 102
2. The hair and its basal cell .............................................. 102
3. Gradation in size of cells from cortex to medulla .......................... 103
4. Tetrasporangium ...................................................... 105
5. Carpogonium and its development ...................................... 106
6. Cystocarp and nutritive filaments. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 111
7. Spermatangium and its pattern .... , ...... '" ............................ 112
8. The relationship between Gracilariopsis and Gracilaria .................... 114
D. Key to the species of Gracilaria ............................................ 117
E. Descriptions of species .................................................... 119
1. Subgenus Gracilariella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 119
Gracilaria chorda ...................................................... 119
2. Subgenus Textoriella .................................................. 121
Gracilaria gigas ...................................................... 121
G. blodgettii .......................................................... 122
G. textorii ............................................................ 123
G. incurvata .......................................................... 124
G. punctata .......................................................... 125
G. denticulata ........................................................ 126
G. purpurascens ............................................•......... 127
3. Subgenus Gracilaria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 128
Gracilaria verrucosa .................................................... 128
G. vermiculophylla .................................................... 130
G. arcuata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 131
G. edulis ............................................................ 132
G. coronopifolia ...................................................... 133
G. sublittoralis ........................................................ 133
4,. Species of uncertain position ............................................ 135
Gracilaria salicornia ......................................... , ........ 135
G. eucheumioides ...................................................... 136
F. Discussion ................................................................ 136
G. Summary ................................................................ 137
H. Literature................................................................ 138
* Contribution No. 21 from the Usujiri Fisheries Laboratory, Faculty of Fisheries, Hokkaido
University.
- 97 -
Mem. Fac. Fish. Hokkaido Univ. [XXV, 2
Abbreviations used in the present paper
a: apical cell. p: procarp.
aux: auxiliary cell. psm: primordium of spermatangial
ca: carposporangium. mother cell.
cb: carpogonial branch. sc: spermatangial conceptacle.
cbi: carpogonial branch initial. sm: spermatium.
cbp: carpogonial branch primordium. sp: spermatangium.
cp: carpogonium. spmc: spermatangial mother cell.
fu: fusion cell. su: supporting cell.
g: gonimoblast. ts: tetrasporangium.
hb: basal cell of hair. tsm: tetrasporangial mother cell.
hy: hypogynous cell. v: vegetative cell.
nf: nutritive filament. ve: ventral side.
A. Introduction
The genus Gracilaria was established by Greville in 1830. He assigned 14
species to this genus, of which the following four are currently retained there:
G. compressa (C. Ag.) Grev. (now G. bursa-pastris (Gmel.) Silva), G. confervoides (L.)
Grev. (now G. verrucosa (Huds.) Papenf.), G. lernanaeformis (Bory) Grev., and G.
Zichenoides (Turn.) Grev. (now G. edulis (Gmel.) Silva). The genus was lectotypified
with G. corifervoides by Schmitz (1889).
J. Agardh revised the genus Gracilaria in 1852 and distinguished three subgenera
on the basis of differences in external form and internal structure.
Early concepts of the species of Gracilaria were mainly based on external form.
However, the nature of the reproductive organs has been considered in the
classification of species since 1926, when Sjostedt revealed the developmental
process of the female reproductive system of three species: G. confervoides, G.
compressa, and G. robusta Setch. According to him, there was no true auxiliary
cell, the carpogonium being the starting point of the fusion cell in all three species.
Nutritive filaments were present in the first two species but absent in the last.
Kylin (1930) considered the lack of nutritive filaments to be of diagnostic value and
described the specimen assigned to G. robusta by Sjostedt as a new species, G.
sjoestedtii. Dawson (1949) regarded nutritive filaments as a diagnostic character
at the generic level and distinguished the genus Gracilariopsis from Gracilaria on
the basis of the absence of nutritive filaments and the small size of the gonimoblast
cells.
In a cytological study of Gracilaria muZtipartita (Clem.) Harv. (now G.
foZiifera (Forssk.) Bjijrg.), Greig-Smith (1954) reported that an auxiliary cell was
produced by the supporting cell of the carpogonial branch and that the connection
between the auxiliary cell and the fertilized carpogonium was made by a short
sporogenous filament. Her observations on the carpogonium and its post
fertilization development were very different from those made by Sjostedt.
In 1966, Papenfuss reported that the presence of nutritive filaments could not
always be confirmed in British material of Gracilaria verrucosa. Consequently
he concluded that the presence of nutritive filaments could not be used as a basis
for separating Gracilaria and Gracilariopsis and thus merged the two genera.
- 98 -
1978] Yamamoto: Study of Gracilaria in Japan
Okamura was the first to study Graoilaria in Japan, recognizing 12 species
between 1916 and 1936, one of which was new. Afterward, Yamada (1938, 1941)
added two more species to the Japanese flora.
Ohmi (1955,1956,1958) made an extensive study of Japanese species, introduc
ing the recent classification proposed by Dawson. In 1958 he gave descriptive
accounts of 15 species and one forma of Graoilaria and of three species of
Graoilariopsis, including one new species described in his previous paper (1956).
Of these species, one each of Gracilaria and Graoilariopsis was new to Japan.
After a period of about ten years, during which very little new information
on the anatomy, systematics, and ecology of Japanese gracilariaceous plants
was made known, the writer (1969, 1973, 1973a, 1973b, 1974) published a series of
papers on the male reproductive organ and on the distribution of the various species
in Hokkaido. Especially the developmental and anatomical studies of the male
reproductive organs of Japanese species have brought to light some features which
seem worthy of consideration for the establishment of the relationship between
Graoilariopsis and Gracilaria. As a result, the writer (1975) concluded that the
genus Gracllariopsis should be merged with the genus Graoilaria, thus agreeing with
Papenfuss (1966), and proposed the recognition of three subgenera on the basis of
the three types of spermatangial patterns.
The present paper presents the results of earlier studies in greater detail than
in previous publications. In addition, an attempt is made to determine whether
the following anatomical and vegetative characters, which have been used to
distinguish the species by many authors in the past, still appear to be of diagnostic
value at the specific level: I, the shape of the circumference of the main axis; 2,
the degree of the constriction at the base of the branch; 3, the gradation in size of
cells from the periphery to the center as observed in cross section; and 4, the
feature of the nutritive filaments in a cystocarp.
This study is based on collections of 16 species made by the writer and
preserved in sea water-formalin.
Before going further, the writer wishes to express his gratitude to Prof. T.
Masaki, Faculty of Fisheries, Hokkaido University, for his kind advice during the
course of the present study and for reading the manuscript. Cordial thanks are due
to Prof. H. Ohmi, Faculty of Fisheries, Hokkaido University, for the loan of his
valuable specimens of Gracilaria and reading the manuscript, and to Dr. T.
Igarashi and Dr. H. Yabu, Faculty of Fisheries, Hokkaido University, for reading
manuscript. Grateful appreciation is extended to Dr. Y. Saito, Faculty of Fisheries,
Hokkaido University, for his encouragement during the present work. The writer
also expresses his thanks to Dr. P. C. Silva, University of California, for correcting
the English and making valuable comments. The writer acknowledges his great
obligation to the following gentlemen for their offer of materials of Gracilaria and
for their kind help during the writer's field trip: Dr. E. Fukuhara, Hokkaido
Regional Fisheries Research Laboratory, Mr. S. Torii, Hokkaido Hakodate Fisheries
Experimental Station, Mr. T. Kaneko, Hokkaido Central Fisheries Experimental
Station, Dr. H. Kito, Tohoku Regional Fisheries Research Laboratory, Dr. N.
Yamada, Shizuoka Prefectural Experiment Station, Mr. S. Sasaki, Hokkaido
Kushiro Fisheries Experimental Station, Dr. M. Ohno, Usa Marine Biological
- 99 -
Mem. Fac. Fish. Hokkaido Univ. [XXV, 2
Station, University of Koehi, Dr. S. Kamura, University of the Ryukyus, Dr. T.
Matsui, Shimonoseki University of Fisheries, Mr, J. Tsukidate, Nansei Regional
Fisheries Research Laboratory, Mr. M. Kakiuchi, Hokkaido Abashiri Fisheries
Experimental Station, Mr. K. Taniguchi, Tohoku Regional Fisheries Research
Laboratory.
B. Materials and methods
1. Collecting places
The writer collected specimens for examination at the following places (Fig.
1): several localities along the coast between Matsumae and Hakodate (including
Cape Shirakami, lzumisawa, Moheji, and Shinori), Usu, Yiido-numa, Akkeshi
Lagoon, Onne Lagoon, FUren Lagoon, Odaito, Saroma Lagoon, N otoro Lagoon,
Tokoro, Shiribetsu and Oshoro, Hokkaido; Mangoku-ura and Matsukawa-ura, Miyagi
1~ La~n
Saroma
Tokoro ,
f"-( •
• Esash!1 Notoro Lagoon
~Odaito
I,
Filren Lagoon
Onne Lagoon
\ \ Akkeshi Lagoon
Y1ido-numa
___ .
l~USU
•
, -.0 •
•
~
..
<1
•• • l
•
• fI!!-
Okinawa
Fig. 1. Map showing collection sites.
- 100 -
1978] Yamamoto: Study of GTacilaria in Japan
Pref.; Shirahama, Toi and Irozaki,ilzu Pen., Shizuoka Pref.; Shirahama, Wakayama
Pref.; Usa, Kochi Pref.; Arnakusa, Kumamoto Pref.; and Nashiro, Komesu and
Yagachi, Okinawa Pref. Additional specimens, which were also used for the
present study, were sent on the author's request from Esashi, Kitami Prov.,
Hokkaido, Matsushima, Miyagi Pref., Akadama, Sado Prov., Niigata Pref., and
Senzaki Bay, Yamaguchi Pref.
General features of the sea bottom at each locality were noted, serving
as a basis for habitat descriptions for each species.
2. Methods for microscopic observation
Most of the materials was fixed and preserved in 5-8 % sea water-formalin
for anatomical study, but Carnoy's solution was also used for fixation for the
purpose of cytological observations. Sections were made by the freezing microtome
and sometimes squashed preparations were used. Anilin blue and Wittmann's
solution were employed for staining.
The procedure for the measurement of reproductive organs and vegetative cells
SPERMATANGIAL CYSTOCARP
CONCEPTACLE
SPERMATANGIAL
CONCEPTACLE
TETRASPORANGllIVI CELL
Width
Fig. 2. Schemes showing the procedure for measuring reproductive organs and vegetative
cells.
-101-
Mem. Fac. Fish. Hokkaido Univ. [XXV, 2
was as follows (Fig. 2): 1, cystocarpic conceptacles: widths were measured at the
point of maximum external diameter, heights between the conceptacle tip and the
point of greatest basal constriction. 2, spermatangial conceptacles: widths were
measured at the point of maximum internal diameter, depths between the
conceptacle tip and the conceptacle floor. 3; tetrasporangia: widths and heights
were measured at the outside of the cell wall at the point of maximum diameter and
length. 4, cells: lengths and widths were measured in the same manner as in the
tetrasporangia and dimensions are always indicated in the form of length X width
in p.m. For medullary cells, which lack a definite length/width orientation, the
larger measurement is given first.
c.
General considerations
1. External ffYTm of the frcmd and basal constriction of the branch
AB was mentioned in the Introduction, species of Gracilaria were at first
classified solely on the character of the stem - whether cylindrical, partially
compressed, or flattened. Anatomical structure was introduced into the classifica
tion of this genus by J. Agardh (1852-1901).
In 1948, May found that frond shape, which until then had been considered a
stable, genetically fixed character, was rather changeable in some Australian species.
For example, G. lichenoides had been characterized by its cylindrical form, but
May also described a flattened form. Consequently she concluded that external
form was not always a reliable diagnostic character.
Japanese species have been classified generally into two groups depending
upon whether the frond is flattened or cylindrical. The cylindrical species were
further divided into two groups depending upon the degree of constriction at the
base of the branch (Okamura, 1936). The frond form of each of the eight cylindrical
and four flat species described by Okamura has been confirmed by the present
study. As to the basal constriction of the branch, Ohmi (1958) considered the
degree of this constriction to be an important character in distinguishing among
three species: G. verrucosa, G. chfYTda HoLnes, and G. blodgettii Harv. From
personal observation, however, it would seem that this character varies with age
and habitat. Especially in G. verrucosa, branches both with and without a
constriction are often observed in the same frond. Basal constriction of branches is
not pronounced in G. chfYTda, but in G. blodgettii the base of a branch is always
markedly constricted. In Japanese species, at least, this character thus seems
to be of limited diagnostic value.
2. The hair and its basal cell
Rosenvinge (1911) was the first to report the existence of hairs in the genus
Gracilaria. Sjostedt (1926) described their development and structure in G.
bursa-pastf»"is (as G. compressa).
Hairs have been observed in all Japanese species of Gracilaria, although the
frequency of their occurrence varies between individuals. A hair-cell primordium
is a transformed superficial cell, not differing in size from surrounding
vegetative cells in the beginning. A protuberance is produced from the apex of
-102 -
1978] Yamamoto: Study of (kacilaria in Japan
the primordium after enlargement of the cell volume. The protuberance grows
to be a hair which attains a certain length. A constriction takes place at the
base of the hair, so that in the mature condition the hair and its basal cell are
connected by a pit.
A hair contains about 10-15 nuclei in its middle portion or above. Hairs may
be found throughout the frond, but usually occur only in younger portions.
Owing to the ephemeral nature of the hairs, only the basal cells remain in older
" portions of the frond, easily recognized by their large size and densely protoplasmic
content.
The mode of hair formation observed by the writer agrees fundamentally with
that described by Sjostedt. Hairs are sparse, but more or less uniformly distributed
over the frond surface in most Japanese species. In G. punctata (Okam.) Yamada
and G. arcuata Zanard., however, they are grouped in extraordinary sorus-like
assemblages, a discovery made in the present study. In G. punctata the clusters of
basal cells of hairs appear as dark spots to the naked eye (PI. 17, figs. 1,4).
3. GraiJation in size of cells from cortex to medulla
J. Agardh (1901) differentiated series within the subgenera of Gracilaria on the
6. fun:ellatll.
f----=--l---I - 5(a5) 4
--4(a4)
---3(a3)
11
Fig. 3. Diagram showing the vegetative Fig. 4. Semi-logarithmic graph showing
cells in transverse section of frond. the gradation of cell size from out
A and B indicate long and short ermost cell to medulla. .-.: the
diameters respectively. The numbers increased ratio of cell size to out
show the order of cells from out ermost cell; -: the increased ratio
ermost cell to medulla. of cell size to the preceding cell.
-103 -
Mem. Fac. Fish. Hokkaido Univ. [xxV, 2
basis of several structural differences as seen in transverse section of the frond.
Gradation in size of cells from cortex to medulla was used by J. Agardh to dif
ferentiate between two series of species, the Macrocystideae, with an abrupt
change of size, and the Microcystideae, with a gradual change of size. This
character has been used in distinguishing species by several authors (May, 1948;
Dawson, 1949; Ohmi, 1958).
Previously, the rate of change in size of cells has been judged simply from
o
rough observations under the microscope. The writer has attempted to establish
a statistical treatment of cell size in Japanese species. Cell size is expressed as an
area calculated by using the following formulae (Fig. 3):
A+2 B --M , nr2=S
A: cell length; B: cell width; M: mean cell width; r: radius; S: cell size.
The size of each cell in a vertical cell row was compared with that of the
next inner cell and with the outermost cell, respectively, by using the following
formulae (Fig.· 3):
G.gigas
5
G.lldleumioides
6
G. ,errucoll
7
1 2 3 4 5 6 7 8 9 10 11 12 13
cell position cell positill1
Figs. 5-7. Semi-logarithmic graphs showing the gradation of cell size from outermost cell
to medulla. e-e: the increased ratio of cell size to outermost cell; -: the
increased ratio of cell size to the preceding cell.
-104 -
1978] Yamamoto: Study of GTacilaria in Japan
S. vermlculoph,Ua S. blodpttii
8 9
S. chorda
10
4
3
2
Figs. 8-10. Semi-logarithmic graphs showing the gradation of cell size from outermost
cell to medulla. .-.: the increased ratio of cell size to outermost cell; -: the
increased ratio of cell size to the preceding cell.
Sa"+1 R n,
S a" =
~ .... a,,: cell position from the outermost cell; Rn: ratio of size of cell to size
of preceding cell in vertical cell row; Ro: ratio of size of cell to size of outermost
cell in vertical cell row_
When Rn is 4 or less, the transition in cell size is gradual. For example, in G.
furceUata (Mont.) Zanard., an Australian species which May (1948) considered as
having a linear gradation in cell size, measurements taken from May's fig. 9 yield
a value for Rn less than 3. In the Japanese species G. euche:umioides Harv., which
also shows a linear gradation in cell size, the Rn values is somewhat greater than 4
(Fig. 6). Sudden change in cell size is correlated with Rn values of 5 and above.
Statistical examination of 15 Japanese species shows that all except G.
euche:umioides have a sharp demarcation between cortex and medulla, although
there is some variation in the transition rate (Figs. 5-19).
4. Tetrasporangium
Tetrasporangia are scattered over the surface of the frond except in the basal
and apical portions. The primordium is a transformed superficial cell and is not
-105 -